1932

Abstract

Eukaryotic cells are exquisitely responsive to external and internal cues, achieving precise control of seemingly diverse growth processes through a complex interplay of regulatory mechanisms. The budding yeast provides a fascinating model of cell growth in its stress-responsive transition from planktonic single cells to a filamentous pseudohyphal growth form. During pseudohyphal growth, yeast cells undergo changes in morphology, polarity, and adhesion to form extended and invasive multicellular filaments. This pseudohyphal transition has been studied extensively as a model of conserved signaling pathways regulating cell growth and for its relevance in understanding the pathogenicity of the related opportunistic fungus , wherein filamentous growth is required for virulence. This review highlights the broad gene set enabling yeast pseudohyphal growth, signaling pathways that regulate this process, the role and regulation of proteins conferring cell adhesion, and interesting regulatory mechanisms enabling the pseudohyphal transition.

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2021-11-23
2024-12-12
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Literature Cited

  1. 1. 
    Agarwala SD, Blitzblau HG, Hochwagen A, Fink GR. 2012. RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLOS Genet 8:e1002732
    [Google Scholar]
  2. 2. 
    Ahn SH, Acurio A, Kron SJ. 1999. Regulation of G2/M progression by the STE mitogen-activated protein kinase pathway in budding yeast filamentous growth. Mol. Biol. Cell 10:3301–16
    [Google Scholar]
  3. 3. 
    Bao MZ, Schwartz MA, Cantin GT, Yates JR, Madhani H. 2004. Pheromone-dependent destruction of the Tec1 transcription factor is required for MAP kinase signaling specificity in yeast. Cell 119:991–1000
    [Google Scholar]
  4. 4. 
    Bardwell L, Cook JG, Voora D, Baggott DM, Martinez AR, Thorner J. 1998. Repression of yeast Ste12 transcription factor by direct binding of unphosphorylated Kss1 MAPK and its regulation by the Ste7 MEK. Genes Dev 12:2887–98
    [Google Scholar]
  5. 5. 
    Barua S, Li L, Lipke PN, Dranginis AM. 2016. Molecular basis for strain variation in the Saccharomyces cerevisiae adhesin Flo11p. mSphere 1:e00129-16
    [Google Scholar]
  6. 6. 
    Basak A, Query CC. 2014. A pseudouridine residue in the spliceosome core is part of the filamentous growth program in yeast. Cell Rep 8:966–73
    [Google Scholar]
  7. 7. 
    Basu S, González B, Li B, Kimble G, Kozminski KG, Cullen PJ. 2020. Functions for Cdc42p BEM adaptors in regulating a differentiation-type MAP kinase pathway. Mol. Biol. Cell 31:491–510
    [Google Scholar]
  8. 8. 
    Basu S, Vadaie N, Prabhakar A, Li B, Adhikari H et al. 2016. Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise. PNAS 113:E2019–28
    [Google Scholar]
  9. 9. 
    Baur M, Esch RK, Errede B. 1997. Cooperative binding interactions required for function of the Ty1 sterile responsive element. Mol. Cell. Biol. 17:4330–37
    [Google Scholar]
  10. 10. 
    Berman J, Sudbery PE. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet 3:918–31
    [Google Scholar]
  11. 11. 
    Bester MC, Jacobson D, Bauer FF 2012. Many Saccharomyces cerevisiae cell wall protein encoding genes are coregulated by Mss11, but cellular adhesion phenotypes appear only Flo protein dependent. G32131–41
  12. 12. 
    Borneman AR, Leigh-Bell JA, Yu H, Bertone P, Gerstein M, Snyder M. 2006. Target hub proteins serve as master regulators of development in yeast. Genes Dev 20:435–48
    [Google Scholar]
  13. 13. 
    Brandriss MC, Magasanik B. 1979. Genetics and physiology of proline utilization in Saccharomyces cerevisiae: enzyme induction by proline. J. Bacteriol. 140:498–503
    [Google Scholar]
  14. 14. 
    Brito AS, Neuhäuser B, Wintjens R, Marini AM, Boeckstaens M. 2020. Yeast filamentation signaling is connected to a specific substrate translocation mechanism of the Mep2 transceptor. PLOS Genet 16:e1008634
    [Google Scholar]
  15. 15. 
    Brückner S, Schubert R, Kraushaar T, Hartmann R, Hoffmann D et al. 2020. Kin discrimination in social yeast is mediated by cell surface receptors of the Flo11 adhesin family. eLife 9:e55587
    [Google Scholar]
  16. 16. 
    Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR 2009. Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. PNAS 106:18321–26
    [Google Scholar]
  17. 17. 
    Bumgarner SL, Neuert G, Voight BF, Symbor-Nagrabska A, Grisafi P et al. 2012. Single-cell analysis reveals that noncoding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment. Mol. Cell 45:470–82
    [Google Scholar]
  18. 18. 
    Cain CW, Lohse MB, Homann OR, Sil A, Johnson AD. 2012. A conserved transcriptional regulator governs fungal morphology in widely diverged species. Genetics 190:511–21
    [Google Scholar]
  19. 19. 
    Celenza JL, Carlson M. 1984. Cloning and genetic mapping of SNF1, a gene required for expression of glucose-repressible genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:49–53
    [Google Scholar]
  20. 20. 
    Chan CXJ, El-Kirat-Chatel S, Joseph IG, Jackson DN, Ramsook CB et al. 2016. Force sensitivity in Saccharomyces cerevisiae flocculins. mSphere 1:e00128-16
    [Google Scholar]
  21. 21. 
    Chan CXJ, Lipke PN. 2014. Role of force-sensitive amyloid-like interactions in fungal catch bonding and biofilms. Eukaryot. Cell 13:1136–42
    [Google Scholar]
  22. 22. 
    Chant J, Pringle JR. 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol 129:751–65
    [Google Scholar]
  23. 23. 
    Chapa-y-Lazo B, Allwood EG, Smaczynska-de Rooij II, Snape ML, Ayscough KR. 2014. Yeast endocytic adaptor AP-2 binds the stress sensor Mid2 and functions in polarized cell responses. Traffic 15:546–57
    [Google Scholar]
  24. 24. 
    Chen H, Fink GR. 2006. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20:1150–61
    [Google Scholar]
  25. 25. 
    Chin BL, Ryan O, Lewitter F, Boone C, Fink GR. 2012. Genetic variation in Saccharomyces cerevisiae: circuit diversification in a signal transduction network. Genetics 192:1523–32
    [Google Scholar]
  26. 26. 
    Choi K, Satterberg B, Lyons DM, Elion E. 1994. Ste5 tethers multiple protein kinases in the MAPK cascade required for mating in S. cerevisiae. Cell 78:499–512
    [Google Scholar]
  27. 27. 
    Chow J, Starr I, Jamalzadeh S, Muniz O, Kumar A et al. 2019. Filamentation regulatory pathways control adhesion-dependent surface responses in yeast. Genetics 212:667–90
    [Google Scholar]
  28. 28. 
    Cook JG, Bardwell L, Thorner J. 1997. Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous growth signalling pathway. Nature 390:85–88
    [Google Scholar]
  29. 29. 
    Cormack BP, Ghori N, Falkow S. 1999. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578–82
    [Google Scholar]
  30. 30. 
    Cullen PJ, Sabbagh W, Graham E, Irick MM, van Olden EK et al. 2004. A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18:1695–708
    [Google Scholar]
  31. 31. 
    Cullen PJ, Sprague GF Jr. 2000. Glucose depletion causes haploid invasive growth in yeast. PNAS 97:13461–63
    [Google Scholar]
  32. 32. 
    Cullen PJ, Sprague GF Jr. 2002. The roles of bud-site-selection proteins during haploid invasive growth in yeast. Mol. Biol. Cell 13:2990–3004
    [Google Scholar]
  33. 33. 
    Cullen PJ, Sprague GF Jr. 2012. The regulation of filamentous growth in yeast. Genetics 190:23–49
    [Google Scholar]
  34. 34. 
    Cutler NS, Pan X, Heitman J, Cardenas ME. 2001. The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol. Biol. Cell 12:4103–13
    [Google Scholar]
  35. 35. 
    Douglas LM, Li L, Yang Y, Dranginis AM 2007. Expression and characterization of the flocculin Flo11/Muc1, a Saccharomyces cerevisiae mannoprotein with homotypic properties of adhesion. Eukaryot. Cell 6:2214–21
    [Google Scholar]
  36. 36. 
    Dranginis AM, Rauceo JM, Coronado JE, Lipke PN. 2007. A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol. . Mol. Biol. Rev. 71:282–94
    [Google Scholar]
  37. 37. 
    Erdman S, Snyder M. 2001. A filamentous growth response mediated by the yeast mating pathway. Genetics 159:919–28
    [Google Scholar]
  38. 38. 
    Finkel JS, Mitchell AP. 2011. Genetic control of Candida albicans biofilm development. Nat. Rev. Microbiol. 9:109–18
    [Google Scholar]
  39. 39. 
    Frøsig MM, Costa SR, Liesche J, Østerberg JT, Hanisch S et al. 2020. Pseudohyphal growth in Saccharomyces cerevisiae involves protein kinase-regulated lipid flippases. J. Cell Sci. 133:jcs235994
    [Google Scholar]
  40. 40. 
    Gavrias V, Andrianopoulos A, Gimeno CJ, Timberlake WE. 1996. Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth. Mol. Microbiol. 19:1255–63
    [Google Scholar]
  41. 41. 
    Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077–90
    [Google Scholar]
  42. 42. 
    Gontar A, Bottema MJ, Binder BJ, Tronnolone H. 2018. Characterizing the shape patterns of dimorphic yeast pseudohyphae. R. Soc. Open Sci. 5:180820
    [Google Scholar]
  43. 43. 
    Gonzalez A, Hall MN. 2017. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J 36:397–408
    [Google Scholar]
  44. 44. 
    Gow NA, Brown AJ, Odds FC. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5:366–71
    [Google Scholar]
  45. 45. 
    Granek JA, Murray D, Kayrkçi O, Magwene PM. 2013. The genetic architecture of biofilm formation in a clinical isolate of Saccharomyces cerevisiae. Genetics 193:587–600
    [Google Scholar]
  46. 46. 
    Grenson M. 1966. Multiplicity of the amino acid permeases in Saccharomyces cerevisiae: II. Evidence for a specific lysine-transporting system. Biochim. Biophys. Acta Gen. Subj. 127:339–46
    [Google Scholar]
  47. 47. 
    Guilliermond A. 1920. The Yeasts New York: John Wiley and Sons, Inc.
    [Google Scholar]
  48. 48. 
    Guo B, Styles CA, Feng Q, Fink GR 2000. A Saccharomyces gene family involved in invasive growth, cell–cell adhesion, and mating. PNAS 97:12158–63
    [Google Scholar]
  49. 49. 
    Halme A, Bumgarner S, Styles CA, Fink GR. 2004. Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116:405–15
    [Google Scholar]
  50. 50. 
    Heitman J, Movva NR, Hall MN. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905–9
    [Google Scholar]
  51. 51. 
    Hoffmann D, Diderrich R, Reithofer V, Friederichs S, Kock M et al. 2020. Functional reprogramming of Candida glabrata epithelial adhesins: the role of conserved and variable structural motifs in ligand binding. J. Biol. Chem. 295:12512–24
    [Google Scholar]
  52. 52. 
    Hong SP, Leiper FC, Woods A, Carling D, Carlson M 2003. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. PNAS 100:8839–43
    [Google Scholar]
  53. 53. 
    Hou J, Tan G, Fink GR, Andrews BJ, Boone C 2019. Complex modifier landscape underlying genetic background effects. PNAS 116:5045–54
    [Google Scholar]
  54. 54. 
    Huang MY, Woolford CA, May G, McManus CJ, Mitchell AP. 2019. Circuit diversification in a biofilm regulatory network. PLOS Pathog 15:e1007787
    [Google Scholar]
  55. 55. 
    Huber A, French SL, Tekotte H, Yerlikaya S, Stahl M et al. 2011. Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L. EMBO J 30:3052–64
    [Google Scholar]
  56. 56. 
    Hughes Hallett JE, Luo X, Capaldi AP 2015. Snf1/AMPK promotes the formation of Kog1/Raptor-bodies to increase the activation threshold of TORC1 in budding yeast. eLife 4:e09181
    [Google Scholar]
  57. 57. 
    Jaiswal D, Turniansky R, Green EM. 2017. Choose your own adventure: the role of histone modifications in yeast cell fate. J. Mol. Biol. 429:1946–57
    [Google Scholar]
  58. 58. 
    Jansen G, Bühring F, Hollenberg CP, Ramezani Rad M 2001. Mutations in the SAM domain of STE50 differentially influence the MAPK-mediated pathways for mating, filamentous growth and osmotolerance in Saccharomyces cerevisiae. Mol. Genet. Genom. 265:102–17
    [Google Scholar]
  59. 59. 
    Jin R, Dobry CJ, McCown PJ, Kumar A. 2008. Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol. Biol. Cell 19:284–96
    [Google Scholar]
  60. 60. 
    Johnson C, Kweon HK, Sheidy D, Shively CA, Mellacheruvu D et al. 2014. The yeast Sks1p kinase signaling network regulates pseudohyphal growth and glucose response. PLOS Genet 10:e1004183
    [Google Scholar]
  61. 61. 
    Kang S, Choi H. 2005. Effect of surface hydrophobicity on the adhesion of S. cerevisiae onto modified surfaces by poly(styrene-ran-sulfonic acid) random copolymers. Colloids Surf. B. Biointerfaces 46:70–77
    [Google Scholar]
  62. 62. 
    Kapteyn JC, Van Den Ende H, Klis FM. 1999. The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim. Biophys. Acta Gen. Subj. 1426:373–83
    [Google Scholar]
  63. 63. 
    Karunanithi S, Vadaie N, Chavel CA, Birkaya B, Joshi J et al. 2010. Shedding of the mucin-like flocculin Flo11p reveals a new aspect of fungal adhesion regulation. Curr. Biol. 20:1389–95
    [Google Scholar]
  64. 64. 
    Kayikci Ö, Magwene PM 2018. Divergent roles for cAMP-PKA signaling in the regulation of filamentous growth in Saccharomyces cerevisiae and Saccharomyces bayanus. G3 8:3529–38
    [Google Scholar]
  65. 65. 
    Kemp AJ, Betney R, Ciandrini L, Schwenger AC, Romano MC, Stansfield I. 2013. A yeast tRNA mutant that causes pseudohyphal growth exhibits reduced rates of CAG codon translation. Mol. Microbiol. 87:284–300
    [Google Scholar]
  66. 66. 
    Kim HY, Lee SB, Kang HS, Oh GT, Kim T. 2014. Two distinct domains of Flo8 activator mediates its role in transcriptional activation and the physical interaction with Mss11. Biochem. Biophys. Res. Commun. 449:202–7
    [Google Scholar]
  67. 67. 
    Kim J, Rose MD. 2015. Stable pseudohyphal growth in budding yeast induced by synergism between septin defects and altered MAP-kinase signaling. PLOS Genet 11:e1005684
    [Google Scholar]
  68. 68. 
    Kita R, Venkataram S, Zhou Y, Fraser HB. 2017. High-resolution mapping of cis-regulatory variation in budding yeast. PNAS 114:E10736–44
    [Google Scholar]
  69. 69. 
    Kron SJ, Styles CA, Fink GR. 1994. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 5:1003–22
    [Google Scholar]
  70. 70. 
    Kuchin S, Vyas VK, Carlson M. 2002. Snf1 protein kinase and the repressors Nrg1 and Nrg2 regulate FLO11, haploid invasive growth, and diploid pseudohyphal differentiation. Mol. Cell. Biol. 22:3994–4000
    [Google Scholar]
  71. 71. 
    Kunkel J, Luo X, Capaldi AP. 2019. Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast. Nat. Commun. 10:3558
    [Google Scholar]
  72. 72. 
    Kunz J, Henriquez R, Schneider U, Deuter-Reinhard M, Movva NR, Hall MN. 1993. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73:585–96
    [Google Scholar]
  73. 73. 
    Lambrechts MG, Bauer FF, Marmur J, Pretorius IS 1996. Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. PNAS 93:8419–24
    [Google Scholar]
  74. 74. 
    Leberer E, Wu C, Leeuw T, Fourest-Lieuvin A, Segall JE, Thomas DY. 1997. Functional characterization of the Cdc42p binding domain of yeast Ste20p protein kinase. EMBO J 16:83–97
    [Google Scholar]
  75. 75. 
    Lee E, Jung D, Kim J 2020. Roles of Dhh1 RNA helicase in yeast filamentous growth: analysis of N-terminal phosphorylation residues and ATPase domains. J. Microbiol. 58:853–58
    [Google Scholar]
  76. 76. 
    Lee JT, Coradini ALV, Shen A, Ehrenreich IM. 2019. Layers of cryptic genetic variation underlie a yeast complex trait. Genetics 211:1469–82
    [Google Scholar]
  77. 77. 
    Leeuw T, Fourest-Lieuvin A, Wu C, Chenevert J, Clark K et al. 1995. Pheromone response in yeast: association of Bem1p with proteins of the MAP kinase cascade and actin. Science 270:1210–13
    [Google Scholar]
  78. 78. 
    Lenhart BA, Meeks B, Murphy HA 2019. Variation in filamentous growth and response to quorum-sensing compounds in environmental isolates of Saccharomyces cerevisiae. G3 9:1533–44
    [Google Scholar]
  79. 79. 
    Lipke PN. 2018. What we do not know about fungal cell adhesion molecules. J. Fungi 4:59
    [Google Scholar]
  80. 80. 
    Lipke PN, Klotz SA, Dufrene YF, Jackson DN, Garcia-Sherman MC. 2018. Amyloid-like β-aggregates as force-sensitive switches in fungal biofilms and infections. Microbiol. . Mol. Biol. Rev. 82:e00035-17
    [Google Scholar]
  81. 81. 
    Lippman SI, Broach JR 2009. Protein kinase A and TORC1 activate genes for ribosomal biogenesis by inactivating repressors encoded by Dot6 and its homolog Tod6. PNAS 106:19928–33
    [Google Scholar]
  82. 82. 
    Liu H, Styles CA, Fink GR. 1993. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262:1741–44
    [Google Scholar]
  83. 83. 
    Liu H, Styles CA, Fink GR. 1996. Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144:967–78
    [Google Scholar]
  84. 84. 
    Lo H-J, Köhler J, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939–49
    [Google Scholar]
  85. 85. 
    Lo W-S, Dranginis AM. 1996. FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J. Bacteriol. 178:7144–51
    [Google Scholar]
  86. 86. 
    Lo W-S, Dranginis AM. 1998. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9:161–71
    [Google Scholar]
  87. 87. 
    Loeb JDJ, Kerentseva TA, Pan T, Sepulveda-Becerra M, Liu H. 1999. Saccharomyces cerevisiae G1 cyclins are differentially involved in invasive and pseudohyphal growth independent of the filamentation mitogen-activated protein kinase pathway. Genetics 153:1535–46
    [Google Scholar]
  88. 88. 
    Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL et al. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10:457–68
    [Google Scholar]
  89. 89. 
    Lohse MB, Gulati M, Johnson AD, Nobile CJ. 2018. Development and regulation of single- and multi-species Candida albicans biofilms. Nat. Rev. Microbiol. 16:19–31
    [Google Scholar]
  90. 90. 
    Lorenz MC, Cutler NS, Heitman J. 2000. Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol. Biol. Cell 11:183–99
    [Google Scholar]
  91. 91. 
    Lu CF, Kurjan J, Lipke PN. 1994. A pathway for cell wall anchorage of Saccharomyces cerevisiae α-agglutinin. Mol. Cell. Biol. 14:4825–33
    [Google Scholar]
  92. 92. 
    Ma J, Jin R, Jia X, Dobry CJ, Wang L et al. 2007. An interrelationship between autophagy and filamentous growth in budding yeast. Genetics 177:205–14
    [Google Scholar]
  93. 93. 
    Mack D, Nishimura K, Dennehey BK, Arbogast T, Parkinson J et al. 1996. Identification of the bud emergence gene BEM4 and its interactions with Rho-type GTPases in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4387–95
    [Google Scholar]
  94. 94. 
    Madhani HD, Fink GR. 1997. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314–17
    [Google Scholar]
  95. 95. 
    Marcus S, Polverino A, Barr M, Wigler M 1994. Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module. PNAS 91:7762–66
    [Google Scholar]
  96. 96. 
    Mayhew D, Mitra RD. 2014. Transcription factor regulation and chromosome dynamics during pseudohyphal growth. Mol. Biol. Cell 25:2669–76
    [Google Scholar]
  97. 97. 
    Mösch HU, Kübler E, Krappmann S, Fink GR, Braus GH. 1999. Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol. Biol. Cell 10:1325–35
    [Google Scholar]
  98. 98. 
    Mösch HU, Roberts RL, Fink GR 1996. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. PNAS 93:5352–56
    [Google Scholar]
  99. 99. 
    Mutlu N, Sheidy DT, Hsu A, Jeong HS, Wozniak KJ, Kumar A. 2019. A stress-responsive signaling network regulating pseudohyphal growth and ribonucleoprotein granule abundance in Saccharomyces cerevisiae. Genetics 213:705–20
    [Google Scholar]
  100. 100. 
    Nguyen PV, Hlaváĉek O, Maršíkovĉ J, Váchová L, Palkov Z. 2018. Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms. PLOS Genet 14:e1007495
    [Google Scholar]
  101. 101. 
    Nobile CJ, Johnson AD. 2015. Candida albicans biofilms and human disease. Annu. Rev. Microbiol. 69:71–92
    [Google Scholar]
  102. 102. 
    Norman KL, Shively CA, De La Rocha AJ, Mutlu N, Basu S et al. 2018. Inositol polyphosphates regulate and predict yeast pseudohyphal growth phenotypes. PLOS Genet 14:e1007493
    [Google Scholar]
  103. 103. 
    Odds FC. 1985. Morphogenesis in Candida albicans. Crit. Rev. Microbiol. 12:45–93
    [Google Scholar]
  104. 104. 
    Pan X, Heitman J. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:4874–87
    [Google Scholar]
  105. 105. 
    Pan X, Heitman J. 2000. Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol. Cell. Biol. 20:8364–72
    [Google Scholar]
  106. 106. 
    Peeters K, Van Leemputte F, Fischer B, Bonini BM, Quezada H et al. 2017. Fructose-1,6-bisphosphate couples glycolytic flux to activation of Ras. Nat. Commun. 8:922
    [Google Scholar]
  107. 107. 
    Petrova A, Kiktev D, Askinazi O, Chabelskaya S, Moskalenko S et al. 2015. The translation termination factor eRF1 (Sup45p) of Saccharomyces cerevisiae is required for pseudohyphal growth and invasion. FEMS Yeast Res 15:fov033
    [Google Scholar]
  108. 108. 
    Pitoniak A, Chavel CA, Chow J, Smith J, Camara D et al. 2015. Cdc42p-interacting protein Bem4p regulates the filamentous-growth mitogen-activated protein kinase pathway. Mol. Cell. Biol. 35:417–36
    [Google Scholar]
  109. 109. 
    Posas F, Saito H. 1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702–5
    [Google Scholar]
  110. 110. 
    Pothoulakis G, Ellis T. 2018. Synthetic gene regulation for independent external induction of the Saccharomyces cerevisiae pseudohyphal growth phenotype. Commun. Biol. 1:7
    [Google Scholar]
  111. 111. 
    Prabhakar A, Chow J, Siegel AJ, Cullen PJ. 2020. Regulation of intrinsic polarity establishment by a differentiation-type MAPK pathway in S. cerevisiae. J. Cell Sci. 133:jcs241513
    [Google Scholar]
  112. 112. 
    Prinz S, Avila-Campillo I, Aldridge C, Srinivasan A, Dimitrov K et al. 2004. Control of yeast filamentous-form growth by modules in an integrated molecular network. Genome Res 14:380–90
    [Google Scholar]
  113. 113. 
    Pruyne D, Bretscher A. 2000. Polarization of cell growth in yeast. J. Cell Sci. 113:Part 4571–85
    [Google Scholar]
  114. 114. 
    Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6:979–86
    [Google Scholar]
  115. 115. 
    Ramsook C, Tan C, Garcia MC, Fung R, Soybelman G et al. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell 9:393–404
    [Google Scholar]
  116. 116. 
    Renauld H, Aparicio OM, Zierath PD, Billington BL, Chhablani SK, Gottschling DE. 1993. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev 7:1133–45
    [Google Scholar]
  117. 117. 
    Reynolds TB, Fink GR. 2001. Bakers' yeast, a model for fungal biofilm formation. Science 291:878–81
    [Google Scholar]
  118. 118. 
    Roberts RL, Fink GR. 1994. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8:2974–85
    [Google Scholar]
  119. 119. 
    Robertson LS, Fink GR. 1998. The three yeast A kinases have specific signaling functions in pseudohyphal growth. PNAS 95:13783–87
    [Google Scholar]
  120. 120. 
    Rupp S, Summers E, Lo HJ, Madhani H, Fink G. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J 18:1257–69
    [Google Scholar]
  121. 121. 
    Ryan O, Shapiro RS, Kurat CF, Mayhew D, Baryshnikova A et al. 2012. Global gene deletion analysis exploring yeast filamentous growth. Science 337:1353–56
    [Google Scholar]
  122. 122. 
    Schultzhaus Z, Yan H, Shaw BD. 2015. Aspergillus nidulans flippase DnfA is cargo of the endocytic collar and plays complementary roles in growth and phosphatidylserine asymmetry with another flippase, DnfB. Mol. Microbiol 97:18–32
    [Google Scholar]
  123. 123. 
    Sharmeen N, Sulea T, Whiteway M, Wu C. 2019. The adaptor protein Ste50 directly modulates yeast MAPK signaling specificity through differential connections of its RA domain. Mol. Biol. Cell 30:794–807
    [Google Scholar]
  124. 124. 
    Shively CA, Eckwahl MJ, Dobry CJ, Mellacheruvu D, Nesvizhskii A, Kumar A. 2013. Genetic networks inducing invasive growth in Saccharomyces cerevisiae identified through systematic genome-wide overexpression. Genetics 193:1297–310
    [Google Scholar]
  125. 125. 
    Shively CA, Kweon HK, Norman KL, Mellacheruvu D, Xu T et al. 2015. Large-scale analysis of kinase signaling in yeast pseudohyphal development identifies regulation of ribonucleoprotein granules. PLOS Genet 11:e1005564
    [Google Scholar]
  126. 126. 
    Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S et al. 2008. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135:726–37
    [Google Scholar]
  127. 127. 
    Soll DR, Daniels KJ. 2016. Plasticity of Candida albicans biofilms. Microbiol. . Mol. Biol. Rev. 80:565–95
    [Google Scholar]
  128. 128. 
    Song Q, Johnson C, Wilson TE, Kumar A. 2014. Pooled segregant sequencing reveals genetic determinants of yeast pseudohyphal growth. PLOS Genet 10:e1004570
    [Google Scholar]
  129. 129. 
    Stratford M. 1992. Lectin-mediated aggregation of yeasts—yeast flocculation. Biotechnol. Genet. Eng. Rev. 10:283–342
    [Google Scholar]
  130. 130. 
    Taheri N, Kohler T, Braus GH, Mosch HU. 2000. Asymmetrically localized Bud8p and Bud9p proteins control yeast cell polarity and development. EMBO J 19:6686–96
    [Google Scholar]
  131. 131. 
    Toda T, Cameron S, Sass P, Zoller M, Scott JD et al. 1987. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 7:1371–77
    [Google Scholar]
  132. 132. 
    Toda T, Cameron S, Sass P, Zoller M, Wigler M. 1987. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 50:277–87
    [Google Scholar]
  133. 133. 
    Toda T, Uno I, Ishikawa T, Powers S, Kataoka T et al. 1985. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27–36
    [Google Scholar]
  134. 134. 
    Tronnolone H, Gardner JM, Sundstrom JF, Jiranek V, Oliver SG, Binder BJ. 2017. Quantifying the dominant growth mechanisms of dimorphic yeast using a lattice-based model. J. R. Soc. Interface 14:20170314
    [Google Scholar]
  135. 135. 
    Tronnolone H, Tam A, Szenczi Z, Green JEF, Balasuriya S et al. 2018. Diffusion-limited growth of microbial colonies. Sci. Rep. 8:5992
    [Google Scholar]
  136. 136. 
    Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D et al. 2007. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26:663–74
    [Google Scholar]
  137. 137. 
    Vadaie N, Dionne H, Akajagbor DS, Nickerson SR, Krysan DJ, Cullen PJ. 2008. Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J. Cell Biol. 181:1073–81
    [Google Scholar]
  138. 138. 
    Vandermeulen MD, Cullen PJ. 2020. New aspects of invasive growth regulation identified by functional profiling of MAPK pathway targets in Saccharomyces cerevisiae. Genetics 216:95–116
    [Google Scholar]
  139. 139. 
    Verstrepen KJ, Fink GR. 2009. Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Annu. Rev. Genet. 43:1–24
    [Google Scholar]
  140. 140. 
    Verstrepen KJ, Jansen A, Lewitter F, Fink GR. 2005. Intragenic tandem repeats generate functional variability. Nat. Genet. 37:986–90
    [Google Scholar]
  141. 141. 
    Verstrepen KJ, Klis FM. 2006. Flocculation, adhesion and biofilm formation in yeasts. Mol. Microbiol. 60:5–15
    [Google Scholar]
  142. 142. 
    Voordeckers K, De Maeyer D, van der Zande E, Vinces MD, Meert W et al. 2012. Identification of a complex genetic network underlying Saccharomyces cerevisiae colony morphology. Mol. Microbiol. 86:225–39
    [Google Scholar]
  143. 143. 
    Vyas VK, Kuchin S, Berkey CD, Carlson M. 2003. Snf1 kinases with different β-subunit isoforms play distinct roles in regulating haploid invasive growth. Mol. Cell. Biol. 23:1341–48
    [Google Scholar]
  144. 144. 
    Winters MJ, Pryciak PM 2005. Interaction with the SH3 domain protein Bem1 regulates signaling by the Saccharomyces cerevisiae p21-activated kinase Ste20. Mol. Cell. Biol. 25:2177–90
    [Google Scholar]
  145. 145. 
    Wolf JJ, Dowell RD, Mahony S, Rabani M, Gifford DK, Fink GR. 2010. Feed-forward regulation of a cell fate determinant by an RNA-binding protein generates asymmetry in yeast. Genetics 185:513–22
    [Google Scholar]
  146. 146. 
    Wu C, Jansen G, Zhang J, Thomas DY, Whiteway M. 2006. Adaptor protein Ste50p links the Ste11p MEKK to the HOG pathway through plasma membrane association. Genes Dev 20:734–46
    [Google Scholar]
  147. 147. 
    Xu T, Shively CA, Jin R, Eckwahl MJ, Dobry CJ et al. 2010. A profile of differentially abundant proteins at the yeast cell periphery during pseudohyphal growth. J. Biol. Chem. 285:15476–88
    [Google Scholar]
  148. 148. 
    Yang H-Y, Tatebayashi K, Yamamoto K, Saito H. 2009. Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. EMBO J 28:1380–91
    [Google Scholar]
  149. 149. 
    Yang X, Jiang R, Carlson M. 1994. A family of proteins containing a conserved domain that mediates interaction with the yeast SNF1 protein kinase complex. EMBO J 13:5878–86
    [Google Scholar]
  150. 150. 
    Zhou W, Dorrity MW, Bubb KL, Queitsch C, Fields S. 2020. Binding and regulation of transcription by yeast Ste12 variants to drive mating and invasion phenotypes. Genetics 214:397–407
    [Google Scholar]
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